THE MORPHOLOGY, REPRODUCTIVE BIOLOGY AND HABITAT UTILISATION OF THE EXOTIC INVASIVE LIZARD, THE BROWN ANOLE (ANOLIS SAGREI), IN TAIWAN by Gerrut Norval submitted in accordance with the requirements for the degree of MSC In the subject NATURE CONSERVATION at the University of South Africa Supervisor: Dr. Kerry Slater Co-supervisor: Prof. Leslie R. Brown (Date submitted) DECLARATION Student number: 3685-841-2 I declare that THE MORPHOLOGY, REPRODUCTIVE BIOLOGY AND HABITAT UTILISATION OF THE EXOTIC INVASIVE LIZARD, THE BROWN ANOLE (ANOLIS SAGREI), IN TAIWAN is my own work and that all the sources that I have used or quoted have been indicated and acknowledged by means of complete references. 15th of December 2014 ________________________ _____________________ SIGNATURE DATE Mr. Gerrut Norval ([email protected]) Summary Surveys and vegetation analyses were used to determine the known distribution and the characteristics of the habitat utilised by Anolis sagrei in Taiwan. Sampled lizards were used for morphological comparisons, and to investigate the reproductive biology of this species in Taiwan. The results of this study indicate that the distribution of A. sagrei in Taiwan is extensive (≥237 ha) in Chiayi City and County (southwestern study site) and scattered (≥8 ha) in Hualien City and County (eastern study site). These lizards were mostly found in open sunny degraded man-made habitats. Although some variations were noted in the comparisons between the A. sagrei collected from the two study sites, it was concluded that the two populations likely have the same founder population. The reproductive biology study indicated that photoperiod and the associated temperatures determine the reproductive cycles in A. sagrei. It also demonstrated that reproduction in this species is energetically demanding. Key Terms abdominal fat weight cycle; Anolis sagrei; brown anole; habitat preference; human commensal; income breeder; invasive species; liver weight cycle; lizard; photoperiod; reproductive biology Page i TABLE OF CONTENTS SUMMARY…………………………………………………………………………………. i KEY TERMS…………………………………………………………………………………i TABLE OF CONTENT………………………………………………………………………...ii LIST OF FIGURES…………………………………………………………………………...vi LIST OF TABLES…………………………………………………………………………..xiv LIST OF APPENDICES…………………………………………………………………….. xx ACKNOWLEDGEMENTS…………………………………………………………………. xxi CHAPTER 1 – INTRODUCTION……………………………………………………………… 1 1.1. Background to the study…………………………………………………………... 1 1.2. Study species…………………………………………………………………….. 16 1.3. Significance of the study………………………………………………………… 41 1.4. Key questions……………………………………………………………………. 44 1.5. Dissertation outline…………………………………………………………….... 44 1.6. References……………………………………………………………………….. 46 CHAPTER 2 – STUDY AREAS……………………………………………………………... 77 2.1. Introduction……………………………………………………………………… 77 2.2. Study sites………………………………………………………………………...79 2.3. References……………………………………………………………………….. 85 Page ii CHAPTER 3 – MATERIALS AND METHODS……………………………………………….. 88 3.1. Distribution and habitats………………………………………………………… 88 3.1.1. Distribution…………………………………………………………………. 88 3.1.2. Habitat characteristics……………………………………………………….90 3.2. Morphological measurements…………………………………………………… 94 3.3. Reproductive biology……………………………………………………………. 98 3.4. References….…………………………………………………………………... 105 CHAPTER 4 – A DESCRIPTION OF THE KNOWN DISTRIBUTION RANGE OF ANOLIS SAGREI IN TAIWAN AND THE CHARACTERISTICS OF THE HABITATS IT OCCURS IN…………. ………109 4.1. Introduction………………………………………………………………..…… 109 4.2. Results………………………………………………………..………………… 109 4.2.1. Known distribution within study sites……...……………..………………. 109 4.2.2. Vegetation description………………………………………………..…… 111 4.2.3. Plant community classification and descriptions..…………………………114 4.3. Discussion………………………………………………………….…………... 132 4.4. References……………………………………………………………………… 140 CHAPTER 5 – A MORPHOLOGICAL COMPARISON OF ANOLIS SAGREI SPECIMENS FROM SOUTHWESTERN AND EASTERN TAIWAN……………………………………………….. 144 5.1. Introduction………………………………………………………………….…. 144 5.2. Results………………………………………………………………………….. 145 5.3. Discussion……………………………………………………………………… 149 Page iii 5.4. References……………………………………………………………………… 160 CHAPTER 6 – THE REPRODUCTIVE BIOLOGY OF ANOLIS SAGREI FROM SOUTHWESTERN TAIWAN………………………………………………………………………………… 166 6.1. Introduction………………………………………………………………….…. 166 6.2. Results……………………………………………………………………….…. 167 6.2.1. Meteorology………………………………………………………………..167 6.2.2. Sampled specimens………………………………………………………...168 6.2.3. Caudal autotomy…………………………………………………………... 169 6.2.4. Male reproductive cycle…………………………………………………... 171 6.2.5. Male abdominal fat-body weight cycle…………………………………… 174 6.2.6. Male liver weight cycle…………………………………………………… 176 6.2.7. Female reproductive cycle………………………………………………… 177 6.2.8. Female abdominal fat-body weight cycle…………………………………. 178 6.2.9. Female liver weight cycle…………………………………………………. 179 6.3. Discussion……………………………………………………………………… 180 6.4. References……………………………………………………………………… 193 CHAPTER 7 – GENERAL DISCUSSION…………………………………………………… 201 7.1. Discussion………………………………………………………………….…... 201 7.2. Conclusion……………………………………………………………………… 216 7.3. References……………………………………………………………………… 218 Page iv APPENDICES Appendix 4.1. A list of the plant species recorded in the southwestern study site in Chiayi County………………………………………………………………………….. 231 Appendix 4.2. A list of the plant species recorded in the eastern study site in Hualien County…………………………………………………………………………………. 235 Page v List of Figures Chapter 1 Figure 1.1. A striped skink (Trachylepis punctatissima) feeding on raspberry jelly that was dropped on a paved area in an urban garden in Johannesburg, South Africa………………………………………… 3 Figure 1.2. A lateral view of the body (A); the ventral view of the left forelimb and left hind limb (B); a dorsal (C), ventral (D) and lateral (E) view of the head; the dewlap (F); and the cloacal region of an Anolis sagrei male from Santzepu, Chiayi County, southwestern Taiwan.…………………………...………………………………… 23 Figure 1.3. A lateral view of the body (A); the ventral view of the left forelimb and left hind limb (B); a dorsal (C), ventral (D) and lateral (E) view of the head; the dewlap (F); and the cloacal region of an Anolis sagrei female from Santzepu, Chiayi County, southwestern Taiwan..…………………………………………………………….. 24 Figure 1.4. Examples of some of the coloration patterns of Anolis sagrei males from Santzepu, Chiayi County, southwestern Taiwan……………... 26 Figure 1.5. Examples of some of the coloration patterns of Anolis sagrei females from Santzepu, Chiayi County, southwestern Taiwan…….. 27 Figure 1.6. An Anolis sagrei female, captured by a Lycodon ruhstrati ruhstrati, biting the snake (retaliation) in an attempt to escape (A), and an adult Anolis sagrei male that was wedged by a Lanius cristatus Page vi between two wires of a barbed wire fence (B).………….…………. 36 Figure 1.7. A Kiricephalus pattoni nymph (indicated by the red arrow) under the skin of a dissected female Anolis sagrei specimen, collected in Santzepu, southwestern Taiwan…………………………………….. 39 Figure 1.8. An Anolis sagrei male, collected from Chisintang, Hualien County, eastern Taiwan, with an extra foot on the right hind limb………….. 41 Chapter 2 Figure 2.1. A map of Taiwan, indicating the positions of Chiayi County (green shaded area), Chiayi City, Santzepu, Hualien County (orange shaded area), Hualien City, and Chisintang.………………………... 78 Figure 2.2. The monthly mean minimum, mean maximum and mean temperatures (A), monthly mean sunshine duration (B), and monthly mean precipitation (C) of Chiayi County, recorded during the period 1981-2010 (Taiwanese Central Weather Bureau)………. 81 Figure 2.3. The monthly mean minimum, mean maximum and mean temperatures (A), monthly mean sunshine duration (B), and monthly mean precipitation (C) of Hualien County, recorded during the period 1981-2010 (Taiwanese Central Weather Bureau).……… 84 Chapter 3 Figure 3.1. Diagrams illustrating how the snout-vent length (SVL), tail length (TL), head length (HL), and left hind shank length (LHS) were measured……………………………………………………………. 95 Figure 3.2. Images, indicating the (A) mid dorsal scales (Dors. 5 mm; red), Page vii interpariental/interorbital scales (IP/IO; green), interorbital scales (IO; blue), second row of scales between the canthal ridges (2. Canth.; yellow), internasal scales (IN; pink), (B) mid ventral scales (Ventr. 5 mm; red) enlarged postanal scale (PA; green), (C) supralabial scales (SPL; yellow), second row of loreal scales (red), subocular scales (SO; green), and (D) the lamellae scales under the 4th toe on the left hind foot…………………………………………. 96 Figure 3.3. An aerial view of the agricultural fields, the creek (blue arrow), the cemetery (red arrow), and the plant nursery (green arrow) in Santzepu, Sheishan District, Chiayi County, southwestern Taiwan, where the brown anole (Anolis sagrei) specimens were collected for the reproductive biology study. The localities where the lizards were collected are indicated by green dots (for males) and yellow triangles (for females)………………………………………………. 100 Figure 3.4. During early (A and B) and more advanced stages (C and D) of tail regeneration, the regenerated tails (indicated by red arrows) of Anolis sagrei females (A and C) and males (B and D) can be distinguished from what remains of the original tail by differences in coloration and patterns. Closer examination will also reveal that the scales of an original tail (E) differ from a regenerated tail (F), and the tip of the former is sharper and narrower (G) than that of the latter (H)…………………………………………………………